Thompson, the 100m and 200m Olympic champion from Jamaica, had breezed through the rounds but was way off the pace in the final as the American Bowie, who took Games silver behind Thompson a year ago, charged to gold.
The 26-year-old, a member of the United States team that won the Olympic 4x100m title at Rio 2016, launched her body forward to snatch victory from Ivorian rival Mari-Josée Ta Lou by a single hundredth of a second in 10.85sec before tumbling to the ground.
"The dive doesn't feel too good now". "I had no idea", she said.
Olympic champion Elaine Thompson, strangely the only Jamaican in Sunday's final, managed a disappointing 5th with 10.98s.
She trailed Ta Lou by two paces as they headed into the last 20 metres but Bowie just kept charging. Dafne Schippers of the Netherlands won the bronze medal a tenth of a second behind Bowie and Ta Lou. She won her heat in 10.91.
"We didn't have much but she gave us character", added Bowie, who has shortened her name from the unusual Fentorish.
"Honestly I don't know what happened".
"I have a few cuts but I'll be ready for the 200m. Everyone has been running well, so it was going to be hard to get in the medals, so I'm happy to do it".
For Bowie - who finally tasted gold in an individual event after lesser medals in the Olympic 100 and 200m as well as the 2015 100 world final - it will also be a moment of glory shared with her paternal grandmother and her role model, Bobbie Smith.
However, her more battle-hardened compatriot Tori Bowie impressed in her semi-final beating home Ivory Coast's double sprint medallist from the 2013 world championships Murielle Ahoure. "She did what she had to do to get to the line first".
"I think the rest of the world was telling me, why are you choosing the 100 over the 200?"